The role of the Bcl-2 family of apoptosis regulatory proteins in the immune system

Seminars in Immunology

Volumn 9, Issue 1, 1997, Pages 25-33

  Hawkins, Christine J ^a   Vaux, David L ^a  

^a NONE

Author keywords

bcl 2; Cell death; Clonal selection; Cysteine protease; Lymphocyte development

Indexed keywords

CYSTEINE PROTEINASE; PROTEIN BCL 2; REGULATOR PROTEIN;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL DEATH; IMMUNOGENETICS; NONHUMAN; PHYSIOLOGY; PROTO ONCOGENE; TRANSGENIC MOUSE;

EID: 0031079804     PISSN: 10445323     EISSN: None     Source Type: Journal    
DOI: 10.1006/smim.1996.0052     Document Type: Article

References (93)

1. 1. Shortman K, Egerton M, Spangrude GJ, Scollay R (1990) The generation and fate of thymocytes. Semin Immunol 2:3-12
2. 2. Osmond DG (1991) Proliferation kinetics and the lifespan of B cells in central and peripheral lymphoid organs. Curr Opin Immunol 3:179-185
3. 3. Robey EA, Ramsdell F, Kioussis D, Sha W, Loh D, Axel R, Fowles BJ (1992) The level of CD8 expression can determine the outcome of thymic selection. Cell 69:1089-1096
4. 4. Surh CD, Sprent J (1994) T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 372:100-103
5. 5. Smith CA, Williams GT, Kingston R, Jenkinson EJ, Owen JJ (1989) Antibodies to CD3/ T-cell receptor complex induce death by apoptosis in immature T cells in thymic cultures. Nature 337:181-184
6. 6. Nossal GJ (1994) Negative selection of lymphocytes. Cell 76:229-239
7. 7. Strasser A (1995) Apoptosis - death of a T cell. Nature 373:385-386
8. 8. Russell JH, Rush B, Weaver C, Wang R (1993) Mature T cells of autoimmune 1pr/ 1pr mice have a defect in antigen-stimulated suicide. Proc Natl Acad Sci USA 90:4409-4413
9. 9. Alderson MR, Tough TW, Davis ST, Braddy S, Falk B, Schooley KA, Goodwin RG, Smith CA, Ramsdell F, Lynch DH (1995) Fas ligand mediates activation-induced cell death in human T lymphocytes. J Exp Med 181:71-77
10. 10. Tucekszabo CL, Andjelic S, Lacy E, Elkon KB, Nikolic-Zugic J (1996) Surface T cell Fas receptor/CD95 regulation, in vivo activation, and apoptosis. Activation-induced death can occur without Fas receptor. J Immunol 156:192-200
11. 11. Bakhshi A, Jensen JP, Goldman P, Wright JJ, McBride OW, Epstein AL, Korsmeyer SJ (1985) Cloning the chromosomal breakpoint of t(14;18) human lymphomas: clustering around JH on chromosome 14 and near a transcriptional unit on 18. Cell 41:899-906
12. 12. Bakhshi A, Wright JJ, Graninger W, Seto M, Owens J, Cossman J, Jensen JP, Goldman P, Korsmeyer SJ (1987) Mechanism of the t(14;18) chromosomal translocation: structural analysis of both derivative 14 and 18 reciprocal partners. Proc Natl Acad Sci USA 84:2396-2400
13. 13. Cleary ML, Sklar J (1985) Nucleotide sequence of a t(14;18) chromosomal breakpoint in follicular lymphoma and demonstration of a breakpoint-cluster region near a transcriptionally active locus on chromosome 18. Proc Natl Acad Sci USA 82:7439-7443
14. 14. Tsujimoto Y, Gorham J, Cossman J, Jaffe E, Croce CM (1985) The t(14;18) chromosome translocations involved in B-cell neoplasms result from mistakes in VDJ joining. Science 229:1390-1393
15. 15. Yin XM, Oltval ZN, Korsmeyer SJ (1994) BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature 369:321-323
16. 16. Cory S (1995) Regulation of lymphocyte survival by the Bcl-2 gene family. Annu Rev Immunol 13:513-543
17. 17. HockenberyDM, Zutter MN, Hickey W, Nahm M, Korsmeyer SJ (1991) Bcl-2 protein is topographically restricted in tissues characterized by apoptotic cell death. Proc Natl Acad Sci USA 88:6961-6965
18. 18. Merry DE, Veis DJ, Mickey WF, Korsmeyer SJ (1994) bcl-2 protein expression is widespread in the developing nervous system and retained in the adult PNS. Development 120:301-311
19. 19. Novak DV, Korsmeyer SJ (1994) Bcl-2 protein expression during murine development. Am J Path 145:61-73
20. 20. LeBrun DP, Huie P, Besnier DP, Warnke RA, Sibley RK, Cleary ML (1993) Topographical dissociation of Bcl-2 messenger RNA and protein expression in human lymphoid tissues. Blood 81:293-298
21. 21. LeBrun DP, Warnke RA, Cleary ML (1993) Expression of Bcl-2 in fetal tissues suggests a role in morphogenesis. Am J Pathol 142:743-753
22. 22. Park JR, Bernstein ID, Hockenberg DM (1995) Primitive human hematopoietic precursors express Bcl-x but not Bcl-2. Blood 86:868-876
23. 23. Merino R, Ding L, Veis DJ, Korsmeyer SJ, Nunez G (1994) Developmental regulation of the Bcl-2 protein and susceptibility to cell death in B lymphocytes. EMBO J 13:683-691
24. 24. Oltvai ZN, Milliman CL, Korsmeyer SJ (1993) Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609-619
25. 25. Ohta K, Iwai K, Kasahara Y, Taniguchi N, Krajewski S, Reed JC, Miyawaki T (1995) Immunoblot analysis of cellular expression of Bcl-2 family proteins, Bcl-2, Bax, Bcl-X and Mcl-1, in human peripheral blood and lymphoid tissues. Intl Immunol 7:1817-1825
26. 26. Krajewski S, Krajewska M, Shabaik A, Miyashita T, Wang HG, Reed JC (1994) Immunohistochemical determination of in vivo distribution of Bax, a dominant inhibitor of Bcl-2. Am J Path 145:1323-1336
27. 27. Krajewski S, Krajewska M, Shabaik A, Wang HG, Irie S, Fong L, Reed JC (1994) Immunohistochemical analysis of in vivo patterns of Bcl-x expression. Cancer Res 54:5501-5507
28. 28. Gonzalez-Garcia M, Perez-Ballestero R, Ding L, Duan L, Boise LH, Thompson CB, Nunez G (1994) Bcl-xL is the major Bcl-x mRNA form expressed during murine development and its product localizes to mitochondria. Development 120:3033-3042
29. 29. Ma A, Pena JC, Chang B, Margosian E, Davidson L, Alt FW, Thompson CB (1995) Bcl-x regulates the survival of double-positive thymocytes. Proc Natl Acad Sci USA 92:4763-4767
30. 30. Boise LH, Gonzales-Garcia M, Postema CE, Ding L, Lindsten T, Turka LA, Mao X, Nunez G, Thompson CB (1993) Bcl-x, a Bcl-2 related gene that functions as a dominant regulator of apoptotic cell death. Cell 74:597-608
31. 31. Boise LH, Minn AJ, Noel PJ, June CH, Accavitti MA, Lindsten T, Thompson CB (1995) CD28 costimulation can promote T cell survival by enhancing the expression of Bel-XL. Immunity 3:87-98
32. 32. McDonnell TJ, Deane N, Platt FM, Nunez G, Jaeger U, McKearn JP, Korsmeyer SJ (1989) Bcl-2-immunoglobulin transgenic mice demonstrate extended B cell survival and follicular lymphoproliferation. Cell 57:79-88
33. 33. Strasser A, Harris AW, Vaux DL, Webb E, Bath ML, Adams JM, Cory S (1990) Abnormalities of the immune system induced by dysregulated Bcl-2 expression in transgenic mice. Curr Top Microbiol Immunol 166:175-181
34. 34. Katsumata M, Siegel RM, Louie DC, Miyashita T, Tsujimoto Y, Nowell PC, Greene MI, Reed JC (1992) Differential effects of Bcl-2 on T and B cells in transgenic mice. Proc Natl Acad Sci USA 89:11376-11380
35. 35. Strasser A, Harris AW, Corcoran LM, Cory S (1994) Bcl-2 expression promotes B-but not T-lymphoid development in SCID mice. Nature 368:457-460
36. 36. Karasuyama H, Rolink A, Shinkai Y, Young F, Alt FW, Melchers F (1994) The expression of Vpre-B/ lambda 5 surrogate light chain in early bone marrow precursor B cells of normal and B cell-deficient mutant mice. Cell 77:133-143
37. 37. Strasser A, Harris AW, Cory S (1991) Bcl-2 transgene inhibits T cell death and perturbs thymic self-censorship. Cell 67:889-899
38. 38. Sentman CL, Shutter JR, Hockenbery D, Kanagawa O, Korsmeyer SJ (1991) Bcl-2 inhibits multiple forms of apoptosis but not negative selection in thymocytes. Cell 67:879-888
39. 39. Strasser A, Harris AW, von Boehmer H, Cory S (1994) Positive and negative selection of T cells in T-cell receptor transgenic mice expressing a Bcl-2 transgene. Proc Natl Acad Sci USA 91:1376-1380
40. 40. Linette GP, Grusby MJ, Hedrick SM, Hansen TH, Glimcher LH, Korsmeyer SJ (1994) Bcl-2 is upregulated at the CD4+ CD8+ stage during positive selection and promotes thymocyte differentiation at several control points. Immunity 1:197-205
41. 41. Tao W, Teh SJ, Melhado I, Jirik F, Korsmeyer SJ, Teh HS (1994) The T cell receptor repertoire of CD4-8 + thymocytes is altered by overexpression of the Bcl-2 proto-oncogene in the thymus. J Exp Med 179:145-153
42. 42. Hartley SB, Cooke MP, Fulcher DA, Harris AW, Cory S, Basten A, Goodnow CC (1993) Elimination of self-reactive B lymphocytes proceeds in two stages: arrested development and cell death. Cell 72:325-355
43. 43. Nisitani S, Tsubata T, Murakami M, Okamoto M, Honjo T (1993) The Bcl-2 gene product inhibits clonal deletion of self-reactive B lymphocytes in the periphery but not in the bone marrow. J Exp Med 178:1247-1254
44. 44. Strasser A, Whittingham S, Vaux DL, Bath ML, Adams JM, Cory S, Harris AW (1991) Enforced BCL2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc Natl Acad Sci USA 88:8661-8665
45. 45. Grillot DA, Merino R, Nunez G (1995) Bcl-XL displays restricted distribution during T cell development and inhibits multiple forms of apoptosis but not clonal deletion in transgenic mice. J Exp Med 182:1973-1983
46. 46. Siegel RM, Katsumata M, Miyashita T, Louie DC, Greene MI, Reed JC (1992) Inhibition of thymocyte apoptosis and negative antigenic selection in bcl-2 transgenic mice. Proc Natl Acad Sci USA 89:7003-7007
47. 47. Vaux DL, Aguila HL, Weissman IL (1992) Bcl-2 prevents death of factor-deprived cells but fails to prevent apoptosis in targets of cell mediated killing. Int Immunol 4:821-824
48. 48. Strasser A, Harris AW, Cory S (1993) E mu-bcl-2 transgene facilitates spontaneous transformation of early pre-B and immunoglobulin-secreting cells but not T cells. Oncogene 8:1-9
49. 49. McDonnell TJ, Korsmeyer SJ (1991) Progression from lymphoid hyperplasia to high-grade malignant lymphoma in mice transgenic for the t(14; 18). Nature 349:254-256
50. 50. Vaux DL, Cory S, Adams JM (1988) Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 335:440-442
51. 51. Strasser A, Harris AW, Bath ML, Cory S (1990) Novel primitive lymphoid tumours induced in transgenic mice by cooperation between myc and Bcl-2. Nature 348:331-333
52. 52. Marin MC, Hsu B, Stephens LC, Brisbay S, McDonnel TJ (1995) The functional basis of c-myc and Bcl-2 complementation during multistep lymphomagenesis in vivo. Exp Cell Res 217:240-247
53. 53. Shinto Y, Morimoto M, Katsumata M, Uchida A, Aozasa K, Okamoto M, Kurosawa T, Ochi T, Greene ML, Tsujimoto Y (1995) Moloney murine leukemia virus infection accelerates lymphomagenesis in Eμ-Bcl-2 transgenic mice. Oncogene 11:1729-1736
54. 54. Adams JM, Cory S (1992) Oncogene co-operation in leukaemo-genesis. Cancer Surv 15:119-141
55. 55. Nunez G, Hockenbery D, McDonnell TJ, Sorensen CM, Korsmeyer SJ (1991) Bcl-2 maintains B cell memory. Nature 353:71-73
56. 56. Smith KG, Weiss U, Rajewsky K, Nossal GJ, Tarlinton DM (1994) Bcl-2 increases memory B cell recruitment but does not perturb selection in germinal centers. Immunity 1:803-813
57. 57. Brady H, Salomons GS, Bobeldijk RC, Berns A (1996) T cells from Baxα transgenic mice show accelerated apoptosis in response to stimuli but do not show restored DNA damage-induced cell death in the absence of p53. EMBO J 15:1221-1230
58. 58. Veis DJ, Sorenson CM, Shutter JR, Korsmeyer SJ (1993) Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 75:229-240
59. 59. Nakayama K, Nakayama K, Negishi I, Kuida K, Sawa H, Loh DY (1994) Targeted disruption of Bcl-2αβ in mice: occurrence of gray hair, polycystic kidney disease, and lymphocytopenia. Proc Natl Acad Sci USA 91:3700-3704
60. 60. Kamada S, Shimono A, Shinto Y, Tsujimura T, Takahashi T, Noda T, Kitamura Y, Kondoh H, Tsujimoto Y (1995) Bcl-2 deficiency in mice leads to pleiotropic abnormalities: accelerated lymphoid cell death in thymus and spleen, polycystic kidney, hair hypopigmentation, and distorted small intestine. Cancer Res 55:354-359
61. 61. Nakayama K, Nakayama K, Nagashi I, Kulda K, Shinkai Y, Louie MC, Fields LE, Lucas PJ, Stewart V, Alt FW, Loh DY (1993) Disappearance of the lymphoid system in Bcl-2 homozygous mutant chimeric mice. Science 261:1534-1538
62. 62. Motoyama N, Wang F, Roth KA, Sawa H, Nakayama K, Nakayama K, Negishi I, Senju S, Zhang Q, Fujii S, et al (1995) Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 267:1506-1510
63. 63. Knudson CM, Tung K, Toutellotte WG, Brown G, Korsmeyer SJ (1995) Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270:96-99
64. 64. Lowe SW, Schmitt EM, Smith SW, Osborne BA, Jacks T (1993) p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature 362:847-849
65. 65. Sedlak TW, Oltvai ZN, Yang E, Wang K, Boise LH, Thompson CB, Korsmeyer SJ (1995) Multiple Bcl-2 family members demonstrate selective dimerizations with Bax. Proc Natl Acad Sci USA 92:7834-7838
66. 66. Sato T, Hanada M, Bodrug S, Irie SJ, Iwama N, Boise LH, Thompson CB, Golemis E, Fong L, Wang HG, Reed JC (1994) Interactions among members of the bcl-2 protein family analysed with a yeast two-hybrid system. Proc Natl Acad Sci USA 91:9238-9242
67. 67. Farrow SN, White J, Martinou I, Raven T, Pun KT, Grinham CJ, Martinou JC, Brown R (1995) Cloning of a bcl-2 homologue by interaction with adenovirus e1b 19k. Nature 374:731-733
68. 68. Yang E, Zha J, Jockel J, Boise LH, Thompson CB, Korsmeyer SJ (1995) Bad, a heterodimeric partner for Bcl-xl and Bcl-2, displaces Bax and promotes cell death. Cell 80:285-291
69. 69. Boyd JM, Gallo GJ, Elangovan B, Houghton AB, Malstrom S, Avery BJ, Ebb RG, Subramanian T, Chittenden T, Lutz RJ, et al (1995) Bik, a novel death-inducing protein shares a distinct sequence motif with Bcl-2 family proteins and interacts with viral and cellular survival-promoting proteins. Oncogene 11:1921-1928
70. 70. Boyd JM, Malstrom S, Subramanian T, Venkatesh LJ, Schaeper U, Elangovan B, D'Sa-Eipper C, Chinnadurai G (1994) Adenovirus E1B19kDa and Bcl-2 proteins interact with a common set of cellular proteins. Cell 79:341-351
71. 71. Takayama S, Sato T, Krajewski S, Kochel K, Irie S, Millan JA, Reed JC (1995) Cloning and functional analysis of Bag-1 - a novel Bcl-2-binding protein with anti-cell death activity. Cell 80:279-284
72. 72. Wang HG, Miyashita T, Takayama S, Sato T, Torigoe T, Krajewski S, Tanaka S, Hovey L, Troppmair J, Rapp UR, Reed JC (1994) Apoptosis regulation by interaction of Bcl-2 protein and raf-1 kinase. Oncogene 9:2751-2756
73. 73. Fernandez SM, Bischoff JR (1993) Bcl-2 associates with the ras-related protein R-ras p23. Nature 366:274-275
74. 74. Yin XM, Oltvai ZN, Korsmeyer SJ (1995) Heterodimerization with Bax is required for Bcl-2 to repress cell death. Curr Top Microbiol Immunol 194:331-338
75. 75. Yin XM, Oltvai ZN, Korsmeyer SJ (1994) BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature 369:321-323
76. 76. Cheng E, Levine B, Boise LH, Thompson CB, Hardwick JM (1996) Bax-independent inhibition of apoptosis by Bcl-x(1). Nature 379:554-556
77. 77. Shaham S, Horvitz HR (1996) An alternativeIy spliced C. elegans ced-4 RNA encodes a novel cell death inhibitor. Cell 86:201-208
78. 78. Shaham S, Horvitz HR (1996) Development Caenorhabditis elegans neurons may contain both cell-death protective and killer activities. Genes Dev 10:578-591
79. 79. Kumar S, Harvey NL (1995) The role of multiple cellular proteases in the execution of programmed cell death. FEBS Lett 375:169-173
80. 80. Chinnaiyan AM, Orth K, Orourke K, Duan HJ, Poirier GG, Dixit VM (1996) Molecular ordering of the cell death pathway - Bcl-2 and Bcl-x(1) function upstream of the Ced-3-like apoptotic proteases. J Biol Chem 271:4573-4576
81. 81. Vaux DL (1993) Toward an understanding of the molecular mechanisms of physiological cell death. Proc Natl Acad Sci USA 90:786-789
82. 82. Tsujimoto Y, Croce CM (1986) Analysis of the structure, transcripts, and protein products of bcl-2, the gene involved in human follicular lymphoma. Proc Natl Acad Sci USA 83:5214-5218
83. 83. Hengartner MO, Horvitz HR (1994) C. elegans cell survival gene Ced-9 encodes a functional homolog of the mammalian proto-oncogene Bcl-2. Cell 76:665-676
84. 84. Henderson S, Huen D, Rowe M, Dawson C, Johnson G, Rickinson A (1993) Epstein-Barr virus coded BHRF-1 protein, a viral homolog of Bcl 2, protects human B cells from programmed cell death. Proc Natl Acad Sci USA 90:8479-8483
85. 85. Neilan JG, Lu Z, Afonso CL, Kutish GF, Sussman MD, Rock DL (1993) An African Swine Fever Virus gene with similarity to the proto-oncogene Bcl-2 and the Epstein-Barr virus gene BHRF1. J Virol 67:4391-4394
86. 86. Kozopas KM, Yang T, Buchan HL, Zhou P, Craig RW (1993) Mcl-1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to Bcl-2. Proc Natl Acad Sci USA 90:3516-3520
87. 87. Lin EY Orlofsky A, Berger MS, Prystowsky MB (1993) Characterization of A1, a novel hemopoietic-specific early-response gene with sequence similarity to Bcl-2. J Immunol 151:1979-1988
88. 88. Chittenden T, Harrington EA, Oconnor R, Flemington C, Lutz RJ, Evan GI, Guild BC (1995) Induction of apoptosis by the Bcl-2 homologue Bak. Nature 374:733-736
89. 89. Kiefer MC, Brauer MJ, Powers VC, Wu JJ, Umansky SR, Tomei LD, Barr PJ (1995) Modulation of apoptosis by the widely distributed Bcl-2 homologue Bak. Nature 374:736-739
90. 90. Gillet G, Guerin M, Trembleau A, Brun G (1995) A Bcl-2-related gene is activated in avian cells transformed by the Rous sarcoma virus. EMBO J 14:1372-1381
91. 91. Evans DL, Mansel RE (1995) Molecular evolution and secondary structural conservation in the B-cell lymphoma leukemia 2 (Bcl-2) family of proto-oncogene products. J Mol Evol 41:775-783
92. 92. Zha H, Aime-Sempe C, Sato T, Reed JC (1996) Proapoptotic protein Bax heterodimerises with Bcl-2 homodimerises with Bax via a novel domain (BH3) distinct from BH1 and BH2. J Biol Chem 271:7440-7444
93. 93. Yang E, Korsmeyer SJ (1996) Molecular thanatopsis - a discourse on the Bcl-2 family and cell death. Blood 88:386-401